Transposable element expansion and low-level piRNA silencing in grasshoppers may cause genome gigantism

Liu, Xuanzeng; Muhammad, Majid; Yuan, Hao; Chang, Huihui; Zhao, Lina; Nie, Yimeng; He, Lin; Liu, Xiaojing; He, Xiaoliang; Huang, Yuan

doi:10.1186/s12915-022-01441-w

Cited by 19 publications

(10 citation statements)

References 137 publications

(145 reference statements)

Supporting

Mentioning

Contrasting

Order By: Relevance

“…While the current study includes assembly lengths up to 4100 Mb, flow cytometry data shows evidence of insect genomes exceeding 18,000 Mb ( Bryodemella holdereri , Cong et al 2022). Insect models have potential to offer new insights on genome gigantism as assemblies for additional large-genome species become available (Liu et al 2022). With high species diversity and broad distributions in nearly all habitat types, insects may be particularly useful for understanding factors driving temporal dynamics of TE activity including population demographics (Schrader et al 2014) and environmental stress (Horváth et al 2017; Signor et al 2022).…”

Section: Discussionmentioning

confidence: 99%

600+ insect genomes reveal repetitive element dynamics and highlight biodiversity-scale repeat annotation challenges

Sproul

Hotaling

Heckenhauer

et al. 2022

Preprint

View full text Add to dashboard Cite

Repetitive elements (REs) are integral to the composition, structure, and function of eukaryotic genomes. Yet, RE dynamics remain understudied in many taxonomic groups, preventing holistic understanding of how genomes and species evolve. Here, we investigated REs across 601 insect species (20 orders) to better understand the RE landscape of insects and to evaluate automated RE annotation methods in the era of biodiversity genomics. We identified wide variation in the types and frequency of REs across insect groups. We quantified associations between REs and protein-coding genes and found an elevated frequency of associations in insects with abundant long interspersed nuclear elements (LINEs). Sequencing technology impacts RE detection; ~36% more REs could be identified in long-read versus short-read assemblies. Long terminal repeats (LTRs) showed markedly improved detection in long-read assemblies (162% more), while DNA transposons and LINEs showed less respective technology-related bias. We illustrate fundamental challenges to efficient study of REs in diverse groups, showing that in most insect lineages, 25-85% of repetitive sequences were unclassified compared to only ~13% of unclassified repeats in Drosophila species. Our findings suggest this RE-annotation bottleneck, driven largely by uneven taxonomic representation in RE reference databases, is worsening. Although the diversity of available insect genomes has rapidly expanded, the rate of community contributions to RE databases (essential for RE annotation) has not kept pace, preventing high resolution study of REs in most groups. We highlight the tremendous opportunity and need for the field of biodiversity genomics to embrace REs and suggest collective steps for making progress towards this goal.

show abstract

Section: Discussionmentioning

confidence: 99%

600+ insect genomes reveal repetitive element dynamics and highlight biodiversity-scale repeat annotation challenges

Sproul

Hotaling

Heckenhauer

et al. 2022

Preprint

View full text Add to dashboard Cite

show abstract

“…A few studies in invertebrates have begun to reveal differences in TE and silencing dynamics in genomes of different sizes. In a pairwise comparison of grasshopper species with different genome sizes, Liu et al revealed that the species with the larger genome had higher TE expression, lower piRNA abundance, and lower expression of the piRNA biogenesis gene HENMT, which suggested that lower piRNA-mediated TE silencing was permissive to higher TE activity and genome expansion (Liu et al, 2022). A comparison between Drosophila melanogaster and the mosquito Aedes aegypti, which has a larger genome (1.38 Gb versus 180 Mb), revealed that the mosquito has a higher TE load and a smaller percentage of TEmapping piRNAs (Arensburger et al, 2011).…”

Section: The Te-silencing Arms Race Dynamic Across Genome Sizesmentioning

confidence: 99%

Transposable element and host silencing activity in gigantic genomes

Wang

Yuan

Tang

et al. 2023

Front. Cell Dev. Biol.

View full text Add to dashboard Cite

Transposable elements (TEs) and the silencing machinery of their hosts are engaged in a germline arms-race dynamic that shapes TE accumulation and, therefore, genome size. In animal species with extremely large genomes (>10 Gb), TE accumulation has been pushed to the extreme, prompting the question of whether TE silencing also deviates from typical conditions. To address this question, we characterize TE silencing via two pathways—the piRNA pathway and KRAB-ZFP transcriptional repression—in the male and female gonads of Ranodon sibiricus, a salamander species with a ∼21 Gb genome. We quantify 1) genomic TE diversity, 2) TE expression, and 3) small RNA expression and find a significant relationship between the expression of piRNAs and TEs they target for silencing in both ovaries and testes. We also quantified TE silencing pathway gene expression in R. sibiricus and 14 other vertebrates with genome sizes ranging from 1 to 130 Gb and find no association between pathway expression and genome size. Taken together, our results reveal that the gigantic R. sibiricus genome includes at least 19 putatively active TE superfamilies, all of which are targeted by the piRNA pathway in proportion to their expression levels, suggesting comprehensive piRNA-mediated silencing. Testes have higher TE expression than ovaries, suggesting that they may contribute more to the species’ high genomic TE load. We posit that apparently conflicting interpretations of TE silencing and genomic gigantism in the literature, as well as the absence of a correlation between TE silencing pathway gene expression and genome size, can be reconciled by considering whether the TE community or the host is currently “on the attack” in the arms race dynamic.

show abstract

“…A few studies in invertebrates have begun to reveal differences in TE and silencing dynamics in genomes of different sizes. In a pairwise comparison of grasshopper species with different genome sizes, Liu et al revealed that the species with the larger genome had higher TE expression, lower piRNA abundance, and lower expression of the piRNA biogenesis gene HENMT , which suggested that lower piRNA-mediated TE silencing was permissive to higher TE activity and genome expansion (Liu et al, 2022). A comparison between Drosophila melanogaster and the mosquito Aedes aegypti , which has a larger genome (1.38 Gb versus 180 Mb), revealed that the mosquito has a higher TE load and a smaller percentage of TE-mapping piRNAs (Arensburger et al, 2011).…”

Section: Discussionmentioning

confidence: 99%

Transposable element and host silencing activity in gigantic genomes

Wang

Yuan

Tang

et al. 2022

Preprint

View full text Add to dashboard Cite

Transposable elements (TEs) and the silencing machinery of their hosts are engaged in a germline arms-race dynamic that shapes TE accumulation and, therefore, genome size. In animal species with extremely large genomes (>10 Gb), TE accumulation has been pushed to the extreme, prompting the question of whether TE silencing also deviates from typical conditions. To address this question, we characterize TE silencing via two pathways -- the piRNA pathway and KRAB-ZFP transcriptional repression -- in the male and female gonads of Ranodon sibiricus, a salamander species with a ~21 Gb genome. We quantify 1) genomic TE diversity, 2) TE expression, and 3) small RNA expression and find a significant relationship between the expression of piRNAs and TEs they target for silencing in both sexes. We also quantified TE silencing pathway gene expression in R. sibiricus and 14 other vertebrates with genome sizes ranging from 1 - 130 Gb and find no association between pathway expression and genome size. Taken together, our results reveal that the gigantic R. sibiricus genome includes at least 19 putatively active TE superfamilies, all of which are targeted by the piRNA pathway in proportion to their expression levels, suggesting comprehensive piRNA-mediated silencing. Males have higher TE expression than females, suggesting that they may contribute more to the species' high genomic TE load. We posit that apparently conflicting interpretations of TE silencing and genomic gigantism in the literature, as well as the absence of a correlation between TE silencing pathway gene expression and genome size, can be reconciled by considering whether the TE community or the host is currently on the attack in the arms race dynamic.

show abstract

Transposable element expansion and low-level piRNA silencing in grasshoppers may cause genome gigantism

Cited by 19 publications

References 137 publications

600+ insect genomes reveal repetitive element dynamics and highlight biodiversity-scale repeat annotation challenges

600+ insect genomes reveal repetitive element dynamics and highlight biodiversity-scale repeat annotation challenges

Transposable element and host silencing activity in gigantic genomes

Transposable element and host silencing activity in gigantic genomes

Contact Info

Product

Resources

About